Cortical neuron activation induced by electromagnetic stimulation: a quantitative analysis via modelling and simulation

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• 作者：Tiecheng Wu ; Jie Fan ; Kim Seng Lee ; Xiaoping Li
• 关键词：Neuromodulation ; Pyramidal cell ; Stimulation threshold ; Action potential initiation point ; Computer simulation
• 刊名：Journal of Computational Neuroscience
• 出版年：2016
• 出版时间：February 2016
• 年：2016
• 卷：40
• 期：1
• 页码：51-64
• 全文大小：2,121 KB
• 参考文献：Amassian, V.E., Cracco, R.Q., & Maccabee, P.J. (1989). Focal stimulation of human cerebral cortex with the magnetic coil: a comparison with electrical stimulation. Electroencephalography and Clinical Neurophysiology, 74 (6), 401–416.CrossRef PubMed
  Andres, A.-T., & Andreas, N. (2013). Computationally efficient simulation of electrical activity at cell membranes interacting with self-generated and externally imposed electric fields. Journal of Neural Engineering, 10(2), 026019.CrossRef
  Anwar, H., Riachi, I., Hill, S., Schurmann, F., & Markram, H. (2009). An approach to capturing neuron morphological diversity. In De Schutter, E. (Ed.), Computational Modeling Methods for Neuroscientists. Cambridge: The MIT Press.
  Arlotti, M., Rahman, A., Minhas, P., & Bikson, M. (2012). Axon terminal polarization induced by weak uniform dc electric fields: a modeling study. Conference proceedings :... Annual International Conference of the IEEE Engineering in Medicine and Biology Society. IEEE Engineering in Medicine and Biology Society. Annual Conference, 2012, 4575–8.
  Ascoli, G.A., Donohue, D.E., & Halavi, M. (2007). Neuromorpho.org: a central resource for neuronal morphologies. The Journal of Neuroscience, 27(35), 9247–51.CrossRef PubMed
  Balslev, D., Braet, W., McAllister, C., & Miall, R.C. (2007). Inter-individual variability in optimal current direction for transcranial magnetic stimulation of the motor cortex. Journal of Neuroscience Methods, 162 (1–2), 309–313.CrossRef PubMed
  Barker, A.T., Jalinous, R., & Freeston, I.L. (1985). Non-invasive magnetic stimulation of human motor cortex. The Lancet, 325(8437), 1106–1107.CrossRef
  Berardelli, A., Inghilleri, M., Cruccu, G., & Manfredi, M. (1990). Descending volley after electrical and magnetic transcranial stimulation in man. Neuroscience Letters, 112(1), 54–8.CrossRef PubMed
  Bestmann, S., Baudewig, J., Siebner, H.R., Rothwell, J.C., & Frahm, J. (2003). Subthreshold high-frequency tms of human primary motor cortex modulates interconnected frontal motor areas as detected by interleaved fmri-tms. NeuroImage, 20(3), 1685–96.CrossRef PubMed
  Bikson, M., Inoue, M., Akiyama, H., Deans, J.K., Fox, J.E., Miyakawa, H., & Jefferys, J.G. (2004). Effects of uniform extracellular dc electric fields on excitability in rat hippocampal slices in vitro. Journal of Physiology, 557(Pt 1), 175– 90.PubMedCentral CrossRef PubMed
  Chen, W., Zhang, J.J., Hu, G.Y., & Wu, C.P. (1996). Electrophysiological and morphological properties of pyramidal and nonpyramidal neurons in the cat motor cortex in vitro. Neuroscience, 73(1), 39–55.CrossRef PubMed
  Crank, J., & Nicolson, P. (1947). A practical method for numerical evaluation of solutions of partial differential equations of the heat-conduction type. Proceedings of the Cambridge Philosophical Society, Mathematical and physical sciences, 43, 50–67.CrossRef
  Debanne, D., Campanac, E., Bialowas, A., Carlier, E., & Alcaraz, G. (2011). Axon physiology. Physiological Reviews, 91(2), 555– 602.CrossRef PubMed
  Ding, L., Shou, G., Yuan, H., Urbano, D., & Cha, Y.H. (2014). Lasting modulation effects of rtms on neural activity and connectivity as revealed by resting-state eeg. IEEE Transactions on Biomedical Engineering, 61 (7), 2070–80.CrossRef PubMed
  Esser, S.K., Hill, S.L., & Tononi, G. (2005). Modeling the effects of transcranial magnetic stimulation on cortical circuits. Journal of Neurophysiology, 94(1), 622–639.CrossRef PubMed
  George, M.S., Padberg, F., Schlaepfer, T.E., O’Reardon, J.P., Fitzgerald, P.B., Nahas, Z.H., & Marcolin, M.A. (2009). Controversy: Repetitive transcranial magnetic stimulation or transcranial direct current stimulation shows efficacy in treating psychiatric diseases (depression, mania, schizophrenia, obsessive-complusive disorder, panic, posttraumatic stress disorder). Brain Stimulation, 2(1), 14–21.CrossRef PubMed
  Grill, W.M., Cantrell, M.B., & Robertson, M.S. (2008). Antidromic propagation of action potentials in branched axons: implications for the mechanisms of action of deep brain stimulation. Journal of Computational Neuroscience, 24(1), 81–93.CrossRef PubMed
  Hines, M., & Carnevale, N. (2001). Neuron: a tool for neuroscientists. Neuroscientist, 7, 123–135.CrossRef PubMed
  Inghilleri, M., Berardelli, A., Cruccu, G., & Manfredi, M. (1993). Silent period evoked by transcranial stimulation of the human cortex and cervicomedullary junction. Journal of Physiology, 466, 521–534.PubMedCentral PubMed
  Irnich, W. (1980). The chronaxie time and its practical importance. Pacing and Clinical Electrophysiology : PACE, 3(3), 292–301.CrossRef PubMed
  Jalinous, R. (1991). Technical and practical aspects of magnetic nerve stimulation. Journal of Clinical Neurophysiology, 8(1), 10–25.CrossRef PubMed
  Kamitani, Y., Bhalodia, V.M., Kubota, Y., & Shimojo, S. (2001). A model of magnetic stimulation of neocortical neurons. Neurocomputing, 38-40, 697–703.CrossRef
  Kammer, T., Beck, S., Thielscher, A., Laubis-Herrmann, U., & Topka, H. (2001). Motor thresholds in humans: a transcranial magnetic stimulation study comparing different pulse waveforms, current directions and stimulator types. Clinical Neurophysiology, 112(2), 250–8.CrossRef PubMed
  Lazzaro, V.D., Ziemann, U., & Lemon, R.N. (2008). State of the art: Physiology of transcranial motor cortex stimulation. Brain Stimulation, 1(4), 345–362.CrossRef PubMed
  Mainen, Z., & Sejnowski, T. (1996). Influence of dendritic structure on firing pattern in model neocortical neurons. Nature, 382, 363–366.CrossRef PubMed
  McNeal, D. (1976). Analysis of a model for excitation of myelinated nerve. IEEE Transactions on Biomedical Engineering, 23(4), 329–337.CrossRef PubMed
  Merton, P.A., & Morton, H.B. (1980). Stimulation of the cerebral cortex in the intact human subject. Nature, 285(5762), 227–227.CrossRef PubMed
  Molnár, Z., & Cheung, A.F.P. (2006). Towards the classification of subpopulations of layer v pyramidal projection neurons. Neuroscience Research, 55(2), 105–115.CrossRef PubMed
  Moreines, J.L., McClintock, S.M., & Holtzheimer, P.E. (2011). Neuropsychologic effects of neuromodulation techniques for treatment-resistant depression: a review. Brain Stimulation, 4(1), 17–27.PubMedCentral CrossRef PubMed
  Nagarajan, S.S., Durand, D.M., & Warman, E.N. (1993). Effects of induced electric fields on finite neuronal structures: a simulation study. IEEE Transactions on Biomedical Engineering, 40(11), 1175–88.CrossRef PubMed
  Nakamura, H., Kitagawa, H., Kawaguchi, Y., & Tsuji, H. (1996). Direct and indirect activation of human corticospinal neurons by transcranial magnetic and electrical stimulation. Neuroscience Letters, 210(1), 45–48.CrossRef PubMed
  Pashut, T., Wolfus, S., Friedman, A., Lavidor, M., Bar-Gad, I., Yeshurun, Y., & Korngreen, A. (2011). Mechanisms of magnetic stimulation of central nervous system neurons. PLos Computational Biology, 7(3), e1002022.PubMedCentral CrossRef PubMed
  Pelletier, S.J., & Cicchetti, F. (2015). Cellular and molecular mechanisms of action of transcranial direct current stimulation: evidence from in vitro and in vivo models. The international journal of neuropsychopharmacology / official scientific journal of the Collegium Internationale Neuropsychopharmacologicum (CINP), 18(2).
  Radman, T., Ramos, R.L., Brumberg, J.C., & Bikson, M. (2009). Role of cortical cell type and morphology in subthreshold and suprathreshold uniform electric field stimulation in vitro. Brain Stimulation, 2(4), 215–28, 228 e1–3.PubMedCentral CrossRef PubMed
  Rahman, A., Reato, D., Arlotti, M., Gasca, F., Datta, A., Parra, L.C., & Bikson, M. (2013). Cellular effects of acute direct current stimulation: somatic and synaptic terminal effects. The Journal of physiology, 591(Pt 10), 2563–78.PubMedCentral CrossRef PubMed
  Rattay, F. (1999). The basic mechanism for the electrical stimulation of the nervous system. Neuroscience, 89 (2), 335–46.CrossRef PubMed
  Ridding, M.C., & Rothwell, J.C. (2007). Is there a future for therapeutic use of transcranial magnetic stimulation Nature Reviews Neuroscience, 8(7), 559–67.CrossRef PubMed
  Roth, B.J., & Basser, P.J. (1990). A model of the stimulation of a nerve fiber by electromagnetic induction. IEEE Transactions on Biomedical Engineering, 37(6), 588–97.CrossRef PubMed
  Rothwell, J.C. (1997). Techniques and mechanisms of action of transcranial stimulation of the human motor cortex. Journal of Neuroscience Methods, 74(2), 113–122.CrossRef PubMed
  Rusu, C.V., Murakami, M., Ziemann, U., & Triesch, J. (2014). A model of tms-induced i-waves in motor cortex. Brain Stimulation, 7(3), 401–14.CrossRef PubMed
  Salvador, R., Silva, S., Basser, P.J., & Miranda, P.C. (2011). Determining which mechanisms lead to activation in the motor cortex: a modeling study of transcranial magnetic stimulation using realistic stimulus waveforms and sulcal geometry. Clinical Neurophysiology, 122(4), 748–58.PubMedCentral CrossRef PubMed
  Schulz, R., Gerloff, C., & Hummel, F.C. (2013). Non-invasive brain stimulation in neurological diseases. Neuropharmacology, 64, 579–87.CrossRef PubMed
  Strafella, A.P., Paus, T., Barrett, J., & Dagher, A. (2001). Repetitive transcranial magnetic stimulation of the human prefrontal cortex induces dopamine release in the caudate nucleus. The Journal of Neuroscience, 21(15), RC157.PubMed
  Svirskis, G., Baginskas, A., Hounsgaard, J., & Gutman, A. (1997). Electrotonic measurements by electric field-induced polarization in neurons: theory and experimental estimation. Biophysical Journal, 73(6), 3004–15.PubMedCentral CrossRef PubMed
  Terao, Y., & Ugawa, Y. (2002). Basic mechanisms of tms. Journal of Clinical Neurophysiology, 19(4), 322–43.CrossRef PubMed
  Thielscher, A., & Kammer, T. (2002). Linking physics with physiology in tms: a sphere field model to determine the cortical stimulation site in tms. NeuroImage, 17(3), 1117–30.CrossRef PubMed
  Tranchina, D., & Nicholson, C. (1986). A model for the polarization of neurons by extrinsically applied electric field. Biophysical Journal, 50, 1139–1156.PubMedCentral CrossRef PubMed
  Wang, Y., Gupta, A., Toledo-Rodriguez, M., Wu, C., & Markram, H. (2002). Anatomical, physiological, molecular and circuit properties of nest basket cells in the developing somatosensory cortex. Cerebral Cortex, 12, 395–410.CrossRef PubMed
  Werhahn, K.J., Fong, J.K.Y., Meyer, B.U., Priori, A., Rothwell, J.C., Day, B.L., & Thompson, P.D. (1994). The effect of magnetic coil orientation on the latency of surface emg and single motor unit responses in the first dorsal interosseous muscle. Electroencephalography and Clinical Neurophysiology, 93(2), 138–146.CrossRef PubMed
  Yi, G.S., Wang, J., Wei, X.L., Tsang, K.M., Chan, W.L., Deng, B., & Han, C.X. (2014). Exploring how extracellular electric field modulates neuron activity through dynamical analysis of a two-compartment neuron model. Journal of Computational Neuroscience, 36(3), 383–99.CrossRef PubMed
  
• 作者单位：Tiecheng Wu (1)
  Jie Fan (1) (3)
  Kim Seng Lee (2)
  Xiaoping Li (1)
  
  1. Neuroengineering Laboratory, National University of Singapore, Block EA #04-25, 9 Engineering Drive 1, Singapore, 117576, Singapore
  3. Newrocare Pte Ltd, 6 Eu Tong Sen Street, #12-03, SohoCentral Singapore, 059817, Singapore
  2. Department of Mechanical Engineering, National University of Singapore, Singapore, Singapore
  
• 刊物类别：Biomedical and Life Sciences
• 刊物主题：Biomedicine
  Neurosciences
  Neurology
  Human Genetics
  Theory of Computation
  
• 出版者：Springer Netherlands
• ISSN：1573-6873

文摘

Previous simulation works concerned with the mechanism of non-invasive neuromodulation has isolated many of the factors that can influence stimulation potency, but an inclusive account of the interplay between these factors on realistic neurons is still lacking. To give a comprehensive investigation on the stimulation-evoked neuronal activation, we developed a simulation scheme which incorporates highly detailed physiological and morphological properties of pyramidal cells. The model was implemented on a multitude of neurons; their thresholds and corresponding activation points with respect to various field directions and pulse waveforms were recorded. The results showed that the simulated thresholds had a minor anisotropy and reached minimum when the field direction was parallel to the dendritic-somatic axis; the layer 5 pyramidal cells always had lower thresholds but substantial variances were also observed within layers; reducing pulse length could magnify the threshold values as well as the variance; tortuosity and arborization of axonal segments could obstruct action potential initiation. The dependence of the initiation sites on both the orientation and the duration of the stimulus implies that the cellular excitability might represent the result of the competition between various firing-capable axonal components, each with a unique susceptibility determined by the local geometry. Moreover, the measurements obtained in simulation intimately resemble recordings in physiological and clinical studies, which seems to suggest that, with minimum simplification of the neuron model, the cable theory-based simulation approach can have sufficient verisimilitude to give quantitatively accurate evaluation of cell activities in response to the externally applied field.